Local bradykinin formation is controlled by glycosaminoglycans

Journal of Immunology

Volumn 175, Issue 5, 2005, Pages 3377-3385

  Renné, Thomas ^a,b   Schuh, Kai ^a   Müller Esterl, Werner ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 12; BRADYKININ; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HIGH MOLECULAR WEIGHT KININOGEN; IODINE 125; KALLIKREIN; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; BLOOD VESSEL PERMEABILITY; ENDOTHELIUM CELL; INFLAMMATION; KALLIKREIN KININ SYSTEM; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION;

EID: 23844555133     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.5.3377     Document Type: Article

References (71)

1. Bhoola, K. D., C. D. Figueroa, and K. Worthy. 1992. Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44: 1-80.
2. Colman, R. W., and A. H. Sehmaier. 1997. Contact system: a vascular biology modulator with anticoagulant, profibrinoiytic, antiadhesive, and proinflammatory attributes. Blood 90: 3819-3843.
3. Skidgel, R. A., F. Alhenc-Gelas, and W. B. Campbell. 2003. Prologue: kinins and related systems: new life for old discoveries. Am. J. Physiol 284: H1886-H1891.
4. Ratnoff, O. D., and H. Saito. 1979. Surface-mediated reactions. Curr. Top. Hematol. 1: 1-57.
5. Hojima, Y., C. G. Cochrane, R. C. Wiggins, K. F. Austen, and R. L. Stevens. 1984. In vitro activation of the contact (Hageman factor) system of plasma by heparin and chondroitin sulfate E. Blood 63: 1453-1459.
6. Wiggins, R. C., and C. C. Cochrane. 1979. The autoactivation of rabbit Hageman factor. J. Exp. Med. 150: 1122-1133.
7. Renné, T., J. Dedio, J. C. Meijers, D. Chung, and W. Müller-Esterl. 1999. Mapping of the discontinuous H-kininogen binding site of plasma prekallikrein: evidence for a critical role of apple domain-2. J. Biol. Chem. 274: 25777-25784.
8. Kaplan, A. P., K. Joseph, and M. Silverberg. 2002. Pathways for bradykinin formation and inflammatory disease. J. Allergy Clin. Immunol. 109: 195-209.
9. 2+ stores in rat sympathetic neurons. Proc. Natl. Acad. Sci. USA 95: 7151-7156.
10. Marceau, F., and D. Regoli. 2004. Bradykinin receptor ligands: therapeutic perspectives. Nat. Rev. Drug Discov. 3: 845-852.
11. Leeb-Lundberg, L. M., F. Marceau, W. Müller-Esterl, D. J. Pettibone, and B. L. Zuraw. 2005. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol. Rev. 57: 27-77.
12. Shigematsu, S., S. Ishida, D. C. Gute, and R. J. Korthuis. 2002. Bradykinin-induced proinflammatory signaling mechanisms. Am. J. Physiol. 283: H2676-H2686.
13. Han, E. D., R. C. MacFarlane, A. N. Mulligan, J. Scafidi, and A. E. Davis. III. 2002. Increased vascular permeability in C1 inhibitor-deficient mice mediated by the bradykinin type 2 receptor. J. Clin. Invest. 109: 1057-1063.
14. Proud, D., and A. P. Kaplan. 1988. Kinin formation: mechanisms and role in inflammatory disorders. Annu. Rev. Immunol. 6: 49-83.
15. Nussberger, J., M. Cugno, and M. Cicardi. 2002. Bradykinin-mediated angioedema. N. Engl. J. Med. 347: 621-622.
16. Nussberger, J., M. Cugno, C. Amstutz, M. Cicardi, A. Pellacani, and A. Agostoni. 1998. Plasma bradykinin in angio-oedema. Lancet 351: 1693-1697.
17. Kahn, R., H. Herwald, W. Müller-Esterl, R. Schmitt, A. C. Sjogren. L. Truedsson, and D. Karpman. 2002. Contact-system activation in children with vasculitis. Lancet 360: 535-541.
18. Tilley, S. L., T. M. Coffman, and B. H. Koller. 2001. Mixed messages: modulation of inflammation and immune responses by prostaglandins and thromboxanes. J. Clin. Invest. 108: 15-23.
19. Herwald, H., M. Morgelin, and L. Bjorck. 2003. Contact activation by pathogenic bacteria: a virulence mechanism contributing to the pathophysiology of sepsis. Scand. J. Infect. Dis. 35: 604-607.
20. Persson, K., M. Morgelin, L. Lindbom, P. Aim, L. Bjorck, and H. Herwald. 2000. Severe lung lesions caused by Salmonella are prevented by inhibition of the contact system. J. Exp. Med. 192: 1415-1424.
21. Hasan, A. A., D. B. Cines, H. Herwald, A. H. Schmaier, and W. Müller-Esterl. 1995. Mapping the cell binding site on high molecular weight kininogen domain 5. J. Biol. Chem. 270: 19256-19261.
22. Herwald, H., A. A. Hasan, J. Godovac-Zimmermann, A. H. Schmaier, and W. Müller-Esterl. 1995. Identification of an endothelial cell binding site on kininogen domain D3. J. Biol. Chem. 270: 14634-14642.
23. Bjork, I., S. T. Olson, R. G. Sheffer, and J. D. Shore. 1989. Binding of heparin to human high molecular weight kininogen. Biochemistry 28: 1213-1221.
24. Olson, S. T., R. Sheffer, and A. M. Francis. 1993. High molecular weight kininogen potentiates the heparin-accelerated inhibition of plasma kallikrein by antithrombin: role for antithrombin in the regulation of kallikrein. Biochemistry 32: 12136-12147.
25. Pixley, R. A., Y. Lin, I. Isordia-Salas, and R. W. Colman. 2003. Fine mapping of the sequences in domain 5 of high molecular weight kininogen (HK) interacting with heparin and zinc. J. Thromb. Haemost. 1: 1791-1798.
26. Renné, T., J. Dedio, G. David, and W. Müller-Esterl. 2000. High molecular weight kininogen utilizes heparan sulfate proteoglycans for accumulation on endothelial cells. J. Biol. Chem. 275: 33688-33696.
27. Renné, T., and W. Müller-Esterl. 2001. Cell surface-associated chondroitin sulfate proteoglycans bind contact phase factor H-kininogen. FEBS Lett. 500: 36-40.
28. Bernfield, M., M. Götte, P. Woo Park, O. Reizes, M. L. Fitzgerald, J. Lincecum, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68: 729-777.
29. Yayon, A., M. Klagsbrun, J. D. Esko, P. Leder, and D. M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64: 841-848.
30. Salek-Ardakani, S., J. R. Arrand, D. Shaw, and M. Mackett. 2000. Heparin and heparan sulfate bind interleukin-10 and modulate its activity. Blood 96: 1879-1888.
31. Lortat-Jacob, H., F. Baltzer, and J. A. Grimaud. 1996. Heparin decreases the blood clearance of interferon-γ and increases its activity by limiting the processing of its carboxyl-terminal sequence. J. Biol. Chem. 271: 16139-16143.
32. Lyon, M., G. Rushton, and J. T. Gallagher. 1997. The interaction of the transforming growth factor-βs with heparin/heparan sulfate is isoform-specific. J. Biol. Chem. 272: 18000-18006.
33. Renné, T., D. Gailani, J. C. Meijers, and W. Müller-Esterl. 2002. Characterization of the H-kininogen-binding site on factor XI: a comparison of factor XI and plasma prekallikrein. J. Biol. Chem. 277: 4892-4899.
34. Kaufmann, J., M. Haasemann, S. Modrow, and W. Müller-Esterl. 1993. Structural dissection of the multidomain kininogens: fine mapping of the target epitopes of antibodies interfering with their functional properties. J. Biol. Chem. 268: 9079-9091.
35. Haasemann, M., J. Buschko, A. Faussner, A. A. Roscher, J. Hoebeke, R. M. Burch, and W. Müller-Esterl. 1991. Anti-idiotypic antibodies bearing the internal image of a bradykinin epitope: production, characterization, and interaction with the kinin receptor. J. Immunol. 147: 3882-3892.
36. Motta, G., R. Rojkjaer, A. A. Hasan, D. B. Cines, and A. H. Schmaier. 1998. High molecular weight kininogen regulates prekallikrein assembly and activation on endothelial cells: a novel mechanism for contact activation. Blood 91: 516-528.
37. Adamson, R. H., F. E. Curry, G. Adamson, B. Liu, Y. Jiang, K. Aktories, H. Barth, A. Daigeler, N. Golenhofen, W. Ness, and D. Drenckhahn. 2002. Rho and rho kinase modulation of barrier properties: cultured endothelial cells and intact microvessels of rats and mice. J. Physiol. 539: 295-308.
38. Kozik, A., R. B. Moore, J. Potempa, T. Imamura, M. Rapala-Kozik, and J. Travis. 1998. A novel mechanism for bradykinin production at inflammatory sites: diverse effects of a mixture of neutrophil elastase and mast cell tryptase versus tissue and plasma kallikreins on native and oxidized kininogens. J. Biol. Chem. 273: 33224-33229.
39. David, G., B. van der Schueren, P. Marynen, J. J. Cassiman, and H. van den Berghe. 1992. Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. J. Cell Biol. 118: 961-969.
40. 2 receptor in vivo phosphorylation sites and their role in receptor function. J. Biol. Chem. 276: 40431-40440.
41. Dimmeler, S., I. Fleming, B. Fisslthaler, C. Hermann, R. Busse, and A. M. Zeiher. 1999. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605.
42. 2-HS glycoprotein/fetuin-A: formation of colloidal calciprotein particles. J. Biol. Chem. 278: 13333-13341.
43. Vogel, R., I. Assfalg-Machleidt, A. Esterl, W. Machleidt, and W. Müller-Esterl. 1988. Proteinase-sensitive regions in the heavy chain of low molecular weight kininogen map to the inter-domain junctions. J. Biol. Chem. 263: 12661-12668.
44. Hock, L. R. Vogel, R. P. Linke, and W. Müller-Esterl. 1990. High molecular weight kintnogen-binding site of prekallikrein probed by monoclonal antibodies. J. Biol. Chem. 265: 12005-12011.
45. 2 integrins triggers neutrophil-dependent alteration in endothelial barrier function. J. Exp. Med. 191: 1829-1839.
46. Bossi, F., F. Fisehetti, V. Pellis, R. Bulla, E. Ferrero, T. E. Mollnes, D. Regoli, and F. Tedesco. 2004. Platelet-activating factor and kinin-dependent vascular leakage as a novel functional activity of the soluble terminal complement complex. J. Immunol. 173: 6921-6927.
47. Irie, K., E. Fujii, H. Ishida, K. Wada, T. Suganuma, T. Nishikori, T. Yoshioka, and T. Muraki. 2001. Inhibitory effects of cyclic AMP elevating agents on lipopolysaccharide (LPS)-induced microvascular permeability change in mouse skin. Br. J. Pharmacol. 133: 237-242.
48. Vogel, R., J. Kaufmann, D. W. Chung, J. Kellermann, and W. Müller-Esterl. 1990. Mapping of the prekallikrein-binding site of human H-kininogen by ligand screening of λgt11 expression libraries: mimicking of the predicted binding site by anti-idiotypic antibodies. J. Biol. Chem. 265: 12494-12502.
49. Greengard, J. S., and J. H. Griffin. 1992. High molecular weight kininogen receptor. Methods Enzymol. 215: 369-382.
50. Hulett, M. D., C. Freeman, B. J. Hamdorf, R. T. Baker, M. J. Harris, and C. R. Parish. 1999. Cloning of mammalian heparanase, an important enzyme in tumor invasion and metastasis. Nat. Med. 5: 803-809.
51. Jiang, Y. P., W. Müller-Esterl, and A. H. Schmaier. 1992. Domain 3 of kininogens contains a cell-binding site and a site that modifies thrombin activation of platelets. J. Biol. Chem. 267: 3712-3717.
52. 2 receptor requires phosphorylation of three serine and two threonine residues at its carboxyl tail. J. Biol. Chem. 274: 12738-12747.
53. 2 receptor endocytosis, recycling, and down-regulation assessed using green fluorescent protein conjugates. J. Pharmacol. Exp. Ther. 297: 19-26.
54. Jaspard, E., L. Wei, and F. Alhenc-Gelas. 1993. Differences in the properties and enzymatic specificities of the two active sites of angiotensin I-converting enzyme (kininase II): studies with bradykinin and other natural peptides.-J.-Biol. Chem. 268: 9496-9503.
55. Emanueli, C., E. F. Grady, P. Madeddu, M. Figini, N. W. Bunnett, D. Parisi, D. Regoli, and P. Geppetti. 1998. Acute ACE inhibition causes plasma extravasation in mice that is mediated by bradykinin and substance P. Hypertension 31: 1299-1304.
56. Georgiadis, D., F. Beau, B. Czarny, J. Cotton, A. Yiotakis, and V. Dive. 2003. Roles of the two active sites of somatic angiotensin-converting enzyme in the cleavage of angiotensin I and bradykinin: insights from selective inhibitors. Circ. Res. 93: 148-154.
57. Schapira, M., L. Silver, C. Scott, A. Schmaier, L. Prograis, J. Curd, and R. Colman. 1983. Prekallikrein activation and high molecular weight kininogen consumption in hereditary angioedema. N. Engl. J. Med. 308: 1050-1054.
58. Davis, A. E., III. 2005. The pathophysiology of hereditary angioedema. Clin. Immunol 114: 3-9.
59. Meloni, F. J., E. J. Gustafson, and A. H. Schmaier. 1992. High molecular weight kininogen binds to platelets by its heavy and light chains and when bound has altered susceptibility to kallikrein cleavage. Blood 79: 1233-1244.
60. Herwald, H., M. Morgelin, A. Olsen, M. Rhen, B. Dahlback, W. Müller-Esterl, and L. Bjorck. 1998. Activation of the contact-phase system on bacterial surfaces: a clue to serious complications in infectious diseases. Nat. Med. 4: 298-302.
61. Lin, Y., R. A. Pixley, and R. W. Colman. 2000. Kinetic analysis of the role of zinc in the interaction of domain 5 of high-molecular weight kininogen (HK) with heparin. Biochemistry 39: 5104-5110.
62. Cornelius, R. M., J. Sanchez, P. Olsson, and J. L. Brash. 2003. Interactions of antithrombin and proteins in the plasma contact activation system with immobilized functional heparin. J. Biomed. Mater. Res. 67A: 475-483.
63. Munoz, E. M., and R. J. Linhardt. 2004. Heparin-binding domains in vascular biology. Arterioscler. Thromb. Vasc. Biol. 24: 1549-1557.
64. Borza, D. B., and W. T. Morgan. 1998. Histidine-proline-rich glycoprotein as a plasma pH sensor: modulation of its interaction with glycosaminoglycans by pH and metals. J. Biol. Chem. 273: 5493-5499.
65. 2+ chelation. J. Biol. Chem. 279: 30114-30122.
66. Schmaier, A. H., R. Rojkjaer, and Z. Shariat-Madar. 1999. Activation of the plasma kallikrein/kinin system on cells: a revised hypothesis. Thromb. Haemost. 82: 226-233.
67. Fernando, L. P., Fernando, A. N., and Kaplan, A. P. 2003. Assessment of the role of heparan sulfate in high molecular weight kininogen binding to human umbilical vein endothelial cells. J. Thromb. Haemost. 1: 2444-2449.
68. Shriver, Z., Y. Hu, K. Pojasek, and R. Sasisekharan. 1998. Heparinase II from Flavobacterium heparinum: role of cysteine in enzymatic activity as probed by chemical modification and site-directed mutagenesis. J. Biol. Chem. 273: 22904-22912.
69. Vlodavsky, I., and Y. Friedmann. 2001. Molecular properties and involvement of heparanase in cancer metastasis and angiogenesis. J. Clin. Invest. 108: 341-347.
70. Kurokawa, H., K. Katsube, K. A. Podyma, M. Ikuta, H. Iseki, M. Nakajima, T. Akashi, K. Omura, M. Takagi, and M. Yanagishita. 2003. Heparanase and tumor invasion patterns in human oral squamous cell carcinoma xenografts. Cancer Sci. 94: 277-285.
71. Goldshmidt, O., E. Zcharia, R. Abramovitch, S. Metzger, H. Aingorn, Y. Friedmann, V. Schirrmacher, E. Mitrani, and I. Vlodavsky. 2002. Cell surface expression and secretion of heparanase markedly promote tumor angiogenesis and metastasis. Proc. Natl. Acad. Sci. USA 99: 10031-10036.